The rise of angiosperms pushed conifers to decline during global cooling Fabien L. Condaminea,b,1, Daniele Silvestroc,d,e, Eva B. Koppelhusb, and Alexandre Antonellid,e,f,g aCNRS, UMR 5554 Institut des Sciences de l’Evolution de Montpellier (Université de Montpellier), 34095 Montpellier, France; bDepartment of Biological Sciences, University of Alberta, Edmonton, AB T6G 2E9, Canada; cDepartment of Biology, University of Fribourg, 1700 Fribourg, Switzerland; dDepartment of Biological and Environmental Sciences, University of Gothenburg, SE-405 30 Gothenburg, Sweden; eGothenburg Global Biodiversity Centre, SE-405 30 Gothenburg, Sweden; fDepartment of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, United Kingdom; and gRoyal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE, United Kingdom Edited by Nils Chr. Stenseth, University of Oslo, Oslo, Norway, and approved September 23, 2020 (received for review March 26, 2020) Competition among species and entire clades can impact species When invoking the role of competition in clade replacements, diversification and extinction, which can shape macroevolutionary two main process-based hypotheses can generally explain diver- patterns. The fossil record shows successive biotic turnovers such sification dynamics of entire clades (1, 4, 9). The “passive re- that a dominant group is replaced by another. One striking placement hypothesis” states that an incumbent clade prevents a example involves the decline of gymnosperms and the rapid competing clade from radiating by suppressing speciation, until diversification and ecological dominance of angiosperms in the the incumbent clade declines because of extrinsic factors, such as Cretaceous. It is generally believed that angiosperms outcompeted climate change, thus making the niche space vacant (8). In gymnosperms, but the macroevolutionary processes and alterna- contrast, the “active displacement hypothesis” stipulates that the tive drivers explaining this pattern remain elusive. Using extant rise in diversity of a clade drives the decline of another clade by time trees and vetted fossil occurrences for conifers, we tested the outcompeting it on limited resources and increasing its extinction hypotheses that clade competition or climate change led to the rate (7). Distinguishing between these two hypotheses is even decline of conifers at the expense of angiosperms. Here, we find more challenging for groups that were once ecologically and that both fossil and molecular data show high congruence in taxonomically dominant at the global scale but have either gone revealing 1) low diversification rates, punctuated by speciation extinct or drastically declined in abundance, reducing their – pulses, during warming events throughout the Phanerozoic and 2) ecological role to just a fraction of their past diversity (12 15). EVOLUTION that conifer extinction increased significantly in the Mid- In view of the different drivers that may affect the evolutionary Cretaceous (100 to 110 Ma) and remained high ever since. Their history of a given clade, the question of whether physical changes extinction rates are best explained by the rise of angiosperms, or biotic interactions were responsible for clade replacements is rejecting alternative models based on either climate change or probably best approached by studying individual cases. A notable time alone. Our results support the hypothesis of an active clade example of clade replacement (9) stands within the seed plants replacement, implying that direct competition with angiosperms (Spermatophyta), comprising the gymnosperms and its sister increased the extinction of conifers by pushing their remaining group, the flowering plants (angiosperms). Today, angiosperms species diversity and dominance out of the warm tropics. This represent nearly 90% of all extant plant species and dominate study illustrates how entire branches on the Tree of Life may ac- most of Earth’s terrestrial ecosystems. In contrast, gymnosperms tively compete for ecological dominance under changing climates. account for ∼1% of the total plant diversity and are mostly confined to boreal regions and high-elevation environments, competition | gymnosperms | macroevolution | paleoenvironment even in the tropics (16). How this major pattern of plant diversity nderstanding how competition for resources can regulate Significance Uthe origination and extinction of species and lead to the rise and fall of entire clades represents an important goal of ecology Competition for common resources can make some species and evolutionary biology (1). This is particularly challenging to groups thrive and others decline. Flowering plants rose to study because each clade follows different diversity trajectories dominance between 125 and 80 Ma, undergoing an explosive through time, which are determined by different speciation and radiation that is believed to have impacted long-established extinction regimes that lead clades to rise, decline, or replace plant groups like gymnosperms. Here, we show that the de- one another (2, 3). Paleontological data show evidence of several cline of conifers is strongly and directly linked to the increasing biotic replacements, with once-dominant groups disappearing diversity of flowering plants. Both the fossil record and mo- and others rising to take their place (4–7). lecular data converge in clarifying the effects of abiotic or Two major patterns of clade replacement may be recognized biotic factors on the speciation and extinction rates of conifers. in the fossil record: a double-wedge pattern, in which one clade These results imply that long-term biological interactions declines while the other thrives (e.g., brachiopods and bivalves) through clade competition can play a more important role in (4), and the mass extinction pattern, implying an extinction event the rise and demise of major organism groups than mass that wipes out one group while allowing another to diversify extinctions. (e.g., nonavian dinosaurs and mammals) (8). When two clades of organisms occupy similar habitats and the long-term diversity of Author contributions: F.L.C. designed research; F.L.C. performed research; F.L.C. and D.S. one gradually increases while that of the other declines, we may analyzed data; and F.L.C., D.S., E.B.K., and A.A. wrote the paper. naturally come to the conclusion that a competitive, or negative, The authors declare no competing interest. interaction has taken place between the two (4). However, such a This article is a PNAS Direct Submission. double-wedge pattern could conceivably be produced by differ- This open access article is distributed under Creative Commons Attribution-NonCommercial- ential responses to physical change or differential clade inter- NoDerivatives License 4.0 (CC BY-NC-ND). actions (9). Identifying which abiotic and/or biotic factors control 1To whom correspondence may be addressed. Email: [email protected]. diversity changes is a key challenge in macroevolution (7, 10), This article contains supporting information online at https://www.pnas.org/lookup/suppl/ and macroevolutionary models involving competition as a major doi:10.1073/pnas.2005571117/-/DCSupplemental. driving factor remain disputed (1, 11). www.pnas.org/cgi/doi/10.1073/pnas.2005571117 PNAS Latest Articles | 1of9 Downloaded by guest on September 26, 2021 came into existence over geological time is a long-standing parameters such as global temperatures (53, 54), which are puzzle—Darwin’s “abominable mystery” (17)—and remains a sometimes interlinked (55). Mass extinctions are thought to have topic of intensive research (18–24). Although the timing of the had limited impact on terrestrial plants compared with animal – origin of flowering plants is debated (25 31), there is consensus clades (35, 56, 57); nevertheless, these events acted as important ∼ that they radiated in the Early Cretaceous ( 145 Ma) and are drivers of plant diversity and turnover (58, 59). Each of these the most recently diversifying major clade among the land plants possible drivers, alone or in combination, could explain the wax (25–31). In contrast, gymnosperms appeared well before angio- sperms in the Devonian (∼380 Ma) and flourished in diversity and wane of conifer diversity through time (Fig. 1). during the Mesozoic (14, 32–34). The fossil record shows a To assess a widely held hypothesis that the rise of angiosperms sudden and rapid increase in diversity and geographic spread of drove the decline of gymnosperms (here approximated with co- angiosperms since the middle Cretaceous (18, 19, 35–40), which nifers), we estimate their diversification processes using an in- resulted in the ecological dominance, in terms of species rich- tegrative approach that combines molecular phylogenetics and ness, of flowering plants observed in most terrestrial ecosystems paleontological data. We analyze the available fossil record and today (41–46). As a consequence, it is widely assumed that an- comprehensive dated molecular phylogenies of conifers to tease giosperms underwent such an ecological and evolutionary di- apart the relative impact of angiosperm diversity and climate versification that they outcompeted and outnumbered other land change (here approximated with global temperature and atmo- plants in terms of richness (18, 19, 35–46). Despite decades of spheric carbon) on the diversification of conifers. Given the scientific debate on the pattern of biotic replacements (16–24, 35–39), the main underlying processes of speciation and extinc-